J. Am. Chem. SOC.1995,117, 8051-8052
Photoinduced Electron Transfer within a Donor-Acceptor Pair Juxtaposed by a Salt Bridge James A. Roberts, James P. Kirby, and Daniel G. Nocera*
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Department of Chemistry and LASER Laboratory Michigan State University, East Lansing, Michigan 48824 Received March 6, 1995 The coupling of proton motion to charge separation is a fundamental mechanism in bioenergetic conversions. Energystoring processes of small molecule activation and the translocation of protons across membranes in the proteins and enzymes 11.0 10.0 9.0 8.0 7.0 of photo~ynthesis'-~ and are predicated on protonppm coupled electron transfer (PCET). One approach to investigating Figure 1. 'HNMR spectrum of (bpy)2Ru"(bpy-amidini~m)~+.Selected the mechanism of PCET is to photoinduce electron transfer spectra are shown upon addition of the tetramethylammonium salt of within a donor/acceptor pair that is juxtaposed by proton transfer 3,5-dinitrobenzoate carboxylate at the concentrations 0,0.44,0.89, 2.2, interfaces such as those formed from carboxylic acid dimers8 and 3.1 mM in DMSO-& (bottom to top). The 'Hresonances of the or guanine-cytosine base pairs? For the symmetric -(COOH)2bipyridines appear between 7.3 and 9.2 ppm; two broad singlets flanking interface, proton displacement on one side of the dicarboxylic 9.5 ppm signify the IH resonances of the amidinium protons. For the acid interface is compensated by displacement of a proton from spectrum at 0.44 M carboxylate added, the two resonances are the other side. In this case, proton motion within the interface coincident. influences only the electronic coupling within the donor/acceptor -(COOH)2- interface has been introduced within the donor/ pair and electron transfer is facile.*>I0However, this may not acceptor pair. be the case for asymmetric interfaces where proton motion is accompanied by changes in charge and polarity within the interface. In view of these possible energetic barriers, we wondered whether electron transfer would be coupled to protons in asymmetric interfaces such as salt bridges, which show significant charge redistribution upon proton motion within the interface. One attractive salt bridge for PCET studies is the amidinium-carboxylate interface, which models arginine1 ko, 2 aspartane salt bridges found to be important in many structures including RNA stem loops, zinc finger/DNA c o m p l e ~ e s , ~ ~ , ~ ~ The amidinium-carboxylate salt bridge is fonned directly and the active site of dihydrofolate reductase.I4 But unlike the upon mixing the appropriate carboxylic acid with free base guanidinium-carboxylate interaction of Arg-Asp, amidinium amidine. We have adapted Garigipati's strategyI6 for the shows only one specific binding mode for carboxylate thereby preparation of amidines from nitriles in high yield.I7 Two simplifying PCET studies. We now report the kinetics for 1 in favorable secondary electrostatic interactionsI8 within the amiwhich an electron is transferred from the photoexcited Rudinium-carboxylate interface are manifested in high association ( b ~ y ) 3 ~(bpy + = bipyridine) donor to a 3,5-dinitrobenzene constants even when the solvent is polar. Figure 1 shows the acceptor through an intervening amidinium-carboxylate inter'HNMR spectrum of (bpy)2R~"(bpy-amidinium)~+in DMSOface. This model system was chosen to exploit the well-known d6 at 19.5 OC. The ascending traces highlight the changes in electron transfer chemistry of electronically excited R~(bpy)3~+ the chemical shifts of the amidinium protons, which appear as with nitr0aromati~s.l~1 is compared to 2 where a symmetric broad singlets at -9.5 ppm, upon titration with the tetramethyl(1) Okamura, M. Y.; Feher, G. Annu. Rev. Biochem. 1992, 61, 861. (2) Takahashi, E.; Maroti, P.; Wraight, C. In Electron and Proton Transfer in Chemistry and Biology; Muller, A., Ratajczaks, H., Junge, W., Diemann, E., Eds.; Elsevier: Amsterdam, 1992; pp 219-236. (3)Babcock, G. T.; Barry, B. A.; Debus, R. J.; Hoganson, C. W.; Atamian, M.; McIntosh, L.; Sithole, I.; Yocum, C. F. Biochemistry 1989, 28, 9557. (4) The Photosynthetic Bacterial Reaction CenterStmcture and Dynamics; Breton, J., Vermeglio, A., Eds.; Plenum: New York, 1988. (5) Wikstrom, M. Nature 1989, 338, 776. (6) (a) Babcock, G. T.; Varotsis, C. Proc. SPIE-Znt. SOC.Opt. Eng. 1993, 1890. 104. (b) Babcock. G. T.: Wikstrom. M. Nature 1992.356. 301-309. (7) (a) Malmstrom, B. G. Acc. Chem. Res. 1993,26,332.'(b)Malmstrom, B. G. Chem. Rev. 1990, 90, 1247-1260. (8) Turr6, C.; Chang, C. K.; Leroi, G. E.; Cukier, R. I.; Nocera, D. G. J. Am. Chem. SOC. 1992, 114, 4013. (9) (a) Sessler. J. L.: Wane. B.: Harriman. A. J. Am. Chem. SOC.1993. 115, 10418. (b) Haniman, A, Kubo, Y.; Sessler, J. L. J. Am. Chem. SOC. 1992,114, 388. (10) (a) Cukier, R. I. J. Phys. Chem. 1995, 99, 945. (b) Cukier, R. I. J. Chem. Phys., submitted for publication.. (1 1) Puglisi, J. D.; Chen, L.; Frankel, A. D.; Williamson, J. R. Proc. Natl. Acad. Sa. U.S.A. 1993, 90, 3680-3684. (12) Pavletich, N. P.; Pabo, C. 0. Science 1991, 252, 809. (13)Berg, J. M. Acc. Chem. Res. 1995, 28, 14. (14) Howell, E. H.; Villafranca, J. E.; Warren, M. S.; Oatley, S. J.; Kraut, J. Science 1986, 231, 1125. ( 1 5 ) Bock, C. R.; Connor, J. A.; Gutierrez, A. R.; Meyer, T. J.; Whitten, D. G.; Sullivan, B. P.; Nagle, J. K. J. Am. Chem. SOC.1979, 101, 48154824. (16) Garigipati, R. A. Tetrahedron Lett. 1990, 31, 1969-1972.
ammonium salt of the 3,5-dinitrobenzoate. A concentrationdependent downfield shift of >2.0 ppm is observed for the protons involved in hydrogen bonding to the carboxylate whereas the chemical shift of the adjacent protons, which are not bound to the carboxylate, varies marginally from 9.55 to 9.65 ppm over all concentrations. A least squares fit of a plot of the chemical shift of the hydrogen-bonded amidinium protons vs the carboxylate concentration at 19.5 "C yields Kassoc= 1136 f 93 M-'.I9 Unfortunately, the solubility of 1 in CH2C12, the solvent in which electron transfer kinetics were determined, is too low to permit K,,,,, to be reliably ascertained by NMR titration experiments. Nonetheless we observe the association ( 17) The 4'-methyl-2,2'-bipyridine-4-carboxaldehyde bipyridine (Peek, B. M.; Ross, G. T.; Edwards, S. W.; Meyer, G. J.; Meyer, T. J.; Erickson, B. W. Int. J. Pept. Protein Res. 1991.38, 114) was converted to the nitrile in good yield (70%) following Olah's procedure (Olah, G. A,; Keumi, T. Synthesis 1979, 112). The amidine was obtained from the nitrile by usin Weinreb's amide transfer reagent, methylaluminum(II1) chloroamide.'$ Altematively, the base-catalyzed reaction of the nitrile with methanol afforded the imidate ester, which smoothly reacts with ammonium chloride chloride. The amidiniumto give the 4'-methyl-2,2'-bipyridine-4-amidinium modified bipyridine ligand was reacted with (b~y)2RuC12*2H20 in the usual way. All compounds were characterized by C and 'H NMR and mass spectrometry. (18) (a) Pranata, J.; Wierschke, S. G.; Jorgensen, W. L. J. Am. Chem. Soc. 1991, 113, 2810. (b) Jorgensen, W. L.; Pranata, J. J. Am. Chem. SOC. 1990, 112, 2008.
0002-7863/95/1517-8051$09.00/0 0 1995 American Chemical Society
8052 J. Am. Chem. SOC.,Vol. 117, No. 30,1995 1000 I
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Figure 2. Plot of the concentration-dependent (W) and concentrationindependent ( 0 )decay lifetimes for the quenching of (bpy)2Rur1(bpyamidine)2+ (0.2 mM) by 3,5-DNBCOOH.
constant for 1 to increase with decreasing solvent polarity (K,,, = 2432 M-' in CHsCN at 19.5 "C). On this basis, the DMSO and CH3CN association constants represent a lower limit for the formation of 1 in our electron transfer experiments. For the case of 2, Kass,, measured by techniques previously described by us for the symmetric -(COOH)2- interface: is 702 M-' in CH2Cl2, which is comparable to our previous measurements of a dicarboxylic acid interface bridging a dinitrobenzene acceptor and a porphyrin donor (K,,,, = 552 M-I). The luminescence of (bpy)2R~"(bpy-amidine)~+ in CH2C12 is quenched upon the addition of 3,5-dinitrobenzoic acid (33DNBCOOH). This result is consistent with an electron transfer quenching mechanism, which is well-established for the reaction between electronically excited (Ru")tris(polypyridyl) complexes and nitroaromatic acceptor^.'^ In the absence of 3,5-DNBCOOH, the decay of the (bpy)2R~"(bpy-amidinium)~+excited state is monoexponential with a lifetime of 1300 ns, which decreases upon complexation to aliphatic carboxylates or benzoate (to = 850 ns). However, when 3,5-DNBCOOH is present, a biexponential decay of the luminescence is observed whereupon one lifetime component is dependent on the concentration of acceptor and the other is not over a 3 3 DNBCOOH concentration range of 0.1 -5 mM ([(bpy)2RuI1(bpyamidine)2+] = 0.1 mM) (see Figure 2). The origin of the concentration-dependent decay is easily understood. The Stem-Volmer plot of the concentration-dependent lifetime is linear over the entire quencher concentration range and the intercept is unity. The bimolecular rate constant of 2.4 x lo9 M-' s-' is in accordance with that measured by Meyer et al. for R~(bpy)3~+ and 3,5-dinitrobenzoic acid ET = 1.6 x lo9 M-' s-I).l5 More significantly, the bimolecular kinetics of 1 is similar to that for the reaction of (bpy)2R~"(bpy-amidinium)~+ with the ester 3,5-DNBCOOEt E ET = 1.9 x lo9 M-' s-l ), which is unable to associate with the amidine (association of the amidinium with the nitro functionality is not likely?O which we also confirmed by NMR). The concentration-independent lifetime decay component is attributable to electron transfer for the associated pair shown 1. An intramolecular rate constant of 4.3(9) x IO6 s-l is detennined from the concentrationindependent lifetime decay component. The reaction of (bpy)2R~"(bpy-COOH)~+ with 3,5-DNBCOOH in CHzClz exhibits similar characteristics to the reaction of the quencher with (bpy)2R~I~(bpy-amidine)~+.Lifetime decays are biexponential, also exhibiting concentration-independent and -dependent components. The bimolecular rate constant derived for the latter is 1.4 x lo9 M-ls-l, which is comparable to the reaction rate constant of (bpy)2RuI1(bpyCOOH12+with the ester 3,5-DNBCOOEt ET = 1.1 x lo9 M-' s-l). Despite a 0.07 V smaller driving force (AG(1) = -0.21 V, AG(2) = -0.14 V),21the intramolecular rate constant of 8.0(4) x lo6 s-I for 2 is nearly a factor of 2 greater than that observed for 1. (19) Wilcox, C. S . In Frontiers in Supramolecular Organic Chemistry and Photochemistry; Schneider, H.-J., Durr, H., Eds.; VCH: Weinheim, 1991; pp 123-143. (20) Kelly, T. R.: Kim, M. H. J. Am. Chem. SOC. 1994, 116, 70727080.
Communications to the Editor Does the attenuated PCET process in 1 suggest that the salt bridge is affecting the rate of the ET? To more directly address this issue, we exchanged the 'H atoms of the amidine and carboxylic acid by 2Hand measured the electron transfer kinetics of the associated pair. The intramolecular rate constant for deuterated 1 was 3.2 x lo6 s-I, yielding k ~ / =k 1.34(3). ~ This isotope effect is similar to the kH/kD = 1.5 for 2, and it is consistent with our previous electron transfer measurement of a porphyrin donor-(COOH)2-acceptor complex ( k ~ / = k ~1.6 and 1.7). As recently discussed, a deuterium isotope effect in these hydrogen-bonded systems arises from the modulation of the electronic coupling matrix element by the proton's position within the interface,'0.22thereby providing a mechanism for the asymmetric salt bridge to engender a PCET reaction. The effect of proton motionaon the electron transfer rate may be manifested in ways other than the electronic coupling. Unlike the -(COOH)2- interface, significant charge rearrangement occurs upon proton motion in the salt bridge, and this charge redistribution will couple to solvent (Le., to give rise to additional Franck-Condon factors arising from proton motion).IobMoreover, the electron is transferred through the permanent electrostatic field of the salt bridge thereby modifying the energetics of the overall reaction. These issues may be addressed by comparing the rates of electron transfer for a donor(amidinium-carboxylate)-acceptor complex to those for its congener where the interface is switched (Le., donor-(carboxylate-amidinium)-acceptor). For the systems here, such a comparative study is obscured by the possibility of transferring an electron from the ancillary bipyridine ligand in addition to the transfer of an electron from the derivatized bipyridine ligand because the two metal-to-ligand charge transfer states are close in en erg^.*^,^^ We are therefore currently assessing the issue of PCET rates for switched interface systems with complexes featuring a single bipyridine ligand, and with complexes in which the energy of the metal-to-ligand charge transfer state for the ancillary ligands are energetically far removed from the derivatized amidinium or carboxylate bipyridine ligand. Acknowledgment. The financial support of the National Institutes of Health (GM 47274) is gratefully acknowledged. Supporting Information Available: Fit of the chemical shift data in Figure 1 to obtain K,,,,, representative lifetime decays of the quenching reactions between (bpy)2R~"(bpy-amidine)~+and 3,5DNBCOOH, (bpy)2R~~~(bpy-COOH)~+ and 3J-DNBCOOH, (bpy)2Ru11(bpy-amidine)2+and 3,5-DNBCOOEt, (bpy)2R~"(bpy-COOH)~+ and 3,5-DNBCOOEt, and (bpy)2R~~I(bpy-COOD)~+ and 3,5-DNBCOOD in CH2C12, and Stem-Volmer plots of concentration-dependent decays for (bpy)2R~"(bpy-amidine)~+and 3,5-DNBCOOH, (bpy)2Ru11(bpy-COOH)2+and 3,5-DNBCOOH in CH2C12, (bpy)2Ru"(bpyamidine)2+ and 3,5-DNBCOOEt in CHI&, and (bpy)2Ru11(bpyCOOH)2+ and 3.5-DNBCOOEt in CH2C12 (12 pages). This material is contained in many libraries on microfiche, immediately follows this article in the microfilm version of the joumal, can be ordered from the ACS, and can be downloaded from the Intemet. See any current masthead page for ordering information and Intemet access instructions. JA9507224 (21) Excited state redox potentials of the donors were derived from the free energXrpf the excited state (AGES)and electrochemical measurements of the Ru redox couples. The former was obtained from a spectral fitting of the emission profiles of (bpy)2Ru(bp~-amidine)~+ and (bpy)zRu(bpyCOOH)2+(see: Hupp, J. T.; Neyhart, G. A.; Meyer, T. J.; Kober, E. M. J. Phys. Chem. 1992.96, 10820). The parameters for the fit were EO = 15 649 cm-' and AB112 = 2586 cm-' to yield AG~.q((bpy)2Ru(bpy-amidine)~+') = 2.26 eV and EO = 15,480 cm-' and AVl/2 = 2297 cm-l to give AGs((bpy)zRu(bpy-COOH)2C') = 2.20 eV (Eo is the excited state energy gap and A81/2 is the full width at half-maximum for a single vibronic component). The (bpy)2Ru(bp~-amidine)~+'~+ and (bpy)2R~(bpy-COOH)~+/~+ formal reduction potentials were -1.30 and -1.31 V vs SCE in CH2C12; E1/2(3,5DNBCOOHo/-) is -0.75 V vs SCE. (22)Cukier. R. I. J. Phys. Chem. 1994, 98, 2377. (23) Cooky, L. F.; Headford, C. E. L.; Elliott, C. M.; Kelley, D. F. J. Am. Chem. SOC. 1988, 110, 6673. (24) Opperman, K. A.; Mecklenburg, S. L.; Meyer. T. J. Inorg. Chem. 1994, 33, 5295.
